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Biodiversity patterns of Silurian Radiolaria
Accepted Manuscript Biodiversity patterns of Silurian Radiolaria
Martin Tetard, Claude Monnet, Paula J. Noble, Taniel Danelian PII: DOI: Reference:
S0012-8252(17)30186-1 doi: 10.1016/j.earscirev.2017.07.011 EARTH 2459
To appear in:
Earth-Science Reviews
Received date: Revised date: Accepted date:
5 April 2017 21 June 2017 24 July 2017
Please cite this article as: Martin Tetard, Claude Monnet, Paula J. Noble, Taniel Danelian , Biodiversity patterns of Silurian Radiolaria, Earth-Science Reviews (2017), doi: 10.1016/ j.earscirev.2017.07.011
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ACCEPTED MANUSCRIPT Biodiversity patterns of Silurian Radiolaria
Martin Tetard *, a, b, Claude Monnet a, Paula J. Noble a, c, Taniel Danelian a
Univ. Lille, CNRS, UMR 8198 – Evo-Eco-Paleo, F-59000 Lille, France
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Aix Marseille Univ, CNRS, IRD, Coll France, CEREGE, Aix-en-Provence, France
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University of Nevada, Department of Geological Sciences, Mackay School of Mines, Reno, NV 89557-0138,
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a
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USA
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AUTHOR INFORMATION
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*Corresponding author. Email: [email protected]
Email addresses of all authors: [email protected] (M. Tetard), [email protected] (C. Monnet),
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[email protected] (P.J. Noble), [email protected] (T. Danelian)
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ACCEPTED MANUSCRIPT Abstract Data analysis of all published and well-dated Silurian radiolarian localities was conducted with the goal of revealing long-term patterns in Silurian radiolarian biological diversity. The chronostratigraphic distribution of 161 species was compiled from 25 publications, each selected because of their independent age control. The pattern and dynamics of changes in biodiversity are described using indices that allow for the assessment of changes in taxonomic richness through time. Following the Hirnantian (end-Ordivician) mass extinction, the
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Rhuddanian stage records very low levels of diversity, which then increase gradually throughout the Llandovery series and reach a maximum by the Sheinwoodian stage, before decreasing during the Homerian, and finally,
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rebounding during the Gorstian stage. The early Silurian (Llandovery) appears to be an interval during which
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few species went extinct, although the number of last occurrences increases progressively to reach a peak in the Ludfordian. At the same time first occurrences progressively decrease and are relatively low during the Silurian.
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Only the Gorstian is marked by a sudden increase in origination. The early Silurian is an interval of faunal recovery from the end-Ordovician mass extinction event. Similarly, the Gorstian stage is characterized by a
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recovery following the Homerian low in radiolarian diversity that may be correlated with the C. lundgreni extinction event, which affected a number of other pelagic groups (e.g. graptolites, acritarchs, conodonts, and
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chitinozoans), and with the Mulde event, which coincides with a 4.6‰ positive excursion of the δ13C curve.
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Keywords
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Radiolaria, Paleozoic, paleobiodiversity, macroevolution, biodiversification, taxonomic richness
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ACCEPTED MANUSCRIPT 1. Introduction
Since the appearance of life, Earth’s history has been marked by mass extinctions punctuating periods of relative stability (Raup, 1972, 1976; Sepkoski et al., 1981; Raup and Sepkoski, 1982; Sepkoski, 1984; Alroy, 2008; Alroy et al., 2008; Escarguel et al., 2011). The investigation of such events and of the global mechanisms triggering them may provide some insights into future ecological consequences of our changing world (Alroy et
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al., 2008 and references therein; Sepkoski 1997). Understanding of the Silurian period has evolved over the last few decades (Munnecke et al., 2010). The traditional view for the early Silurian is that of a warm and relatively
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calm period in Earth history, with marine communities progressively recovering from the Hirnantian (end-
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Ordivician) mass extinction (Calner, 2008). However, later studies suggest that the Silurian experienced substantial and rapid climatic and environmental fluctuations, as indicated by the large degree of perturbations
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observed in high resolution C and O isotopic records (Calner, 2008; Munnecke et al., 2010; Gradstein et al., 2012 and references therein), accompanied by major biotic turnovers and extinction events. Many of the biotic
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events cross-cut ecological boundaries and affected well-established groups (Munnecke et al., 2003, 2010; Lenz et al., 2006; Trotter et al., 2016): planktic (acritarchs, graptolites), benthic (brachiopods, trilobites) and nektonic (conodonts), investigation of whose evolution is of primary importance for understanding Silurian
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paleobiodiversity dynamics.
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Most of these groups are also widely used (globally or locally) for Silurian biostratigraphy (Ogg et al., 2016). Marine micro-organisms such as radiolarians represent a significant part of planktic communities at the
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base of marine food webs and are very sensitive to changes in ecological conditions (Lazarus, 2005). Their diversity patterns can thus be used to reconstruct biotic events. However, there are few works that have studied
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radiolarian diversity trends through geological time. The few studies that have been conducted have mainly focused on particular time intervals such as the Permian/Triassic and Cretaceous/Paleogene boundary mass extinctions, or the middle Jurassic to early Cretaceous of the Tethys ocean (Danelian and Johnson, 2001; De Wever et al., 2003; Kiessling and Danelian, 2011). Concerning the Silurian period, most published studies have focused on faunal recovery from the end-Ordovician (Hirnantian) crisis for several groups (e.g. Krug and Patzkowsky, 2004) but excluding the radiolarians. To help fill this knowledge gap, this study focuses on paleodiversity dynamics of the radiolarian faunas during the entire Silurian period. We present a database of Silurian radiolarian occurrences, including a comprehensive dataset at the species level, in order to approximate their standing diversity and to identify
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ACCEPTED MANUSCRIPT biodiversity and evolutionary trends. These patterns are also tested for inherent biases in the database.
2. Material and methods 2.1. Dataset
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A global and exhaustive dataset of Silurian radiolarian occurences was established through surveying the available literature. This survey yielded an inventory of 25 publications that demonstrated sufficient
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chronostratigraphic information to calibrate radiolarian occurrences at the stage level. The constructed dataset
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(Appendix A) contains a list of identified taxa at the species rank for each sample described within a given reference. Samples reported in these references were either dated by fossils other than radiolarians (e.g.
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graptolites) or by absolute dating (e.g. U/Pb SHRIMP). The time calibration of the stages used for the biodiversity analysis is based on the framework established by Ogg et al. (2016). The age of some samples has
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been revised or clarified from the original works when subsequent dating has become available. For example, the age of the Spongocoelia parvus–S. kamitakarensis assemblage regarded by Furutani (1990) as either late Ludlow (in the abstract) or early Ludlow (in the discussion), or mid-Ludlow according to Noble (1994), is here
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considered as late Ludlow based on Nuramkhaan et al. (2013), who made a compelling case for revision. Thus,
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the age of some assemblages may be different from that given in the original publication, but the updated age is always justified by reference to more recent papers. Samples or references were excluded from the analysis if the
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age uncertainty was too large (e.g. Nazarov and Ormiston, 1993) or if most of the specimens were not identified to the species level (e.g. Wakamatsu, 1990; Gorka, 1994; Aitchison et al., 1996; Kurihara and Sashida, 2000b).
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Also, taxonomic assignments of species were reviewed in the original publications and species names were harmonized to remove nomenclatural artifacts that might impede accurate measures of radiolarian diversity. This creates a taxonomic framework that reflects the current state of research with as much consistency and as little redundancy as possible. The final dataset (after cleaning up of uncertain taxa) contains 9 families, 51 genera and 161 species. Most of the data come primarily from Arctic Canada (9 references) and from Japan (7), and sporadically from France, Sweden, Kazakhstan, Texas, Nevada, Alaska, Germany and England (Fig. 1). Therefore, it covers 10 areas, eight of which were situated in tropical paleolatitudes (between 30° N and 30° S) and only two in the midhigh latitudes (near 60° S).
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2.2. Biodiversity metrics
The dataset analyzed in this study (Appendix A) contains only incidence data (i.e. presence/absence) because abundance data are rarely available and were only present in a handful of the surveyed publications. Consequently, biodiversity metrics based on abundance data and correction for sampling bias such as rarefaction
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analyses (Foote, 1992) and subsampling methods (Alroy, 2010) cannot be used in this analysis. This study focuses on taxonomic richness measured at the species rank. The taxa counted herein include also reports of
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species assigned under open nomenclature (e.g. as ‘sp. A’) or with an uncertain specific identification (e.g. ‘cf.’).
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The biodiversity analysis is computed at the chronostratigraphic rank of the eight Silurian stages (Ogg et al., 2016). The choice of these stratigraphic bins was a compromise guided by the resolution required to address our
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research question, the available data, and the maximal precision with which data can be attributed to a given stratigraphic interval of the Silurian (a significant number of references did not date their samples down to the
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biozone).
Biodiversity dynamics through time with incidence data can be estimated by multiple approaches, such as taxonomic richness indices, changes in richness (origination, extinction), and poly-cohort analysis, which are
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processed in this study. The computed analysis was performed by using the scientific environment R (R Core
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Team 2016) version 3.3.0 and with the package ‘epaleo’ (C. Monnet, 2015, unpublished; for applications using this package, see Nowak et al., 2015 and Amberg et al., 2016).
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The actual number of coexisting taxa is the standing diversity, which can only be estimated for paleontological data. Based on incidence taxa, several taxonomic richness indices can be calculated depending
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on the relative weights according to each class of taxa with regard to their occurrence in and around a stratigraphic interval. Taxa are counted as present in a stratigraphic interval in one of four ways (Foote, 2000; Alroy, 2010): as crossovers ranging through the entire interval (sampled or not in it); ranging into and going extinct in that interval; originating within the interval and ranging beyond its upper boundary; and as singleinterval, with a range confined to an interval, meaning that they originate and go extinct within the interval. The sampled-in-bin diversity (Dsib) provides the total count of taxa actually documented from a given stratigraphic interval. This index commonly underestimates diversity due to the incompleteness of the fossil record and sampling bias. Total diversity (Drt-: range-through diversity) also counts all the taxa present in the interval, but it is also calculated by interpolation of discontinuous taxon ranges from established occurrences (Foote, 2000), i.e.
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ACCEPTED MANUSCRIPT taxa not recorded in an interval are counted as being present if they occur in intervals below and above. With this approach, single-interval taxa can be included (Drti) or excluded (Drte). With complete data, total diversity is likely to exceed the standing diversity at any specific point in time, because it does not account for extinctions within an interval (Cooper, 2004). Normalized diversity (Dnorm) is calculated as the number of species ranging throughout the interval (Dover), plus half the number of taxa that originate and/or become extinct in that stage, plus half of those that are confined to the interval itself (D sgl) (Sepkoski, 1975; Cooper, 2004). According to
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Cooper (2004), normalized diversity is a good approximation of the mean standing diversity in a stratigraphic bin.
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Indices of origination and extinction represent, respectively, the number of species originating (Orte and
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Osbe: origination of range-thru excluding single-interval taxa and origination of sampled-in-bin excluding singleinterval taxa, respectively) and becoming extinct (Erte and Esbe) in a stratigraphic interval. Turnover (Trte and Tsbe)
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in an interval is the sum of origination and extinction events, whereas net changes (Crte and Csbe) correspond to origination minus extinction.
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The use of stages as the stratigraphic intervals in this analysis implies that these are inevitably of different durations, which may partly bias diversity counts: longer bins may have a higher taxonomic richness than shorter bins simply because they are sampling longer intervals, while at the same time blurring short-term
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excursions. As the duration of Silurian stages may vary from 1.8 Myr (Gorstian) to 5.1 Myr (Telychian; see Ogg
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et al., 2016) a notable effect may be expected. To correct for a possible bias resulting from these unequal interval lengths, rates per Myr for all diversity indices have been computed. The efficiency of this correction relies on the
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amount and precision of available radio-isotopic ages for this period (see Melchin et al., 2012, fig. 21.12). Poly-cohort analysis is a common tool in paleontology to evaluate evenness of extinction and
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origination rates (Raup, 1978; Foote, 2001; Monnet et al., 2003). Poly-cohort survivorship measures the percentage of species in a cohort, i.e. species present in a given stratigraphic interval that are still present in later intervals. In contrast, poly-cohort prenascence (backward survivorship) measures the proportion of a cohort present in earlier intervals. Poly-cohorts of survivorship and of prenascence are calculated for all stratigraphic bins considered herein. The slope of the cohort curves then represents the rate of extinction or origination for each cohort, with a linear curve (on a logarithmic scale) implying constant rates, while changes over time or between cohorts can reveal changes in rates or biases. The possible influence of sampling bias is evaluated by calculating the Spearman's ρ (rho) and the Kendall’s τ (tau) correlations between the computed diversity indices and the number of studies per interval.
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ACCEPTED MANUSCRIPT These are standard non-parametric rank order correlation coefficients (e.g. Press et al., 1992) commonly used in paleontology (e.g. Dunhill et al., 2012; Na and Kiessling, 2015). The importance of correlation is assessed by Rrho and Rtau values, which vary between -1 and 1 for perfect negative and positive correlation, respectively, with 0 indicating absence of correlation. The statistical significance is given by the probability value p, which is derived from permutation tests. A correlation is accepted as strong if the coefficient is high (> 0.75) and
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significant if the probability value is low (< 0.05).
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3. Results
The constructed dataset used for the biodiversity analysis (Appendix A) contains incidence data (i.e.
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presence/absence) of 161 species distributed in 8 stratigraphic intervals (stages) compiled from 25 source studies (references). The analysis of this dataset enables reconstructing a synthetic occurrence range chart (Appendix B)
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in which species are ordered by family membership and then by appearance, as well as a chart of stratigraphic coverage of source studies (Appendix C). These charts clearly show that some intervals are well documented, such as the Telychian, while other intervals are very poorly studied, such as the Rhuddanian and Ludfordian.
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Also, the synthetic chronostratigraphic range of radiolarian species (Appendix D) shows that on average
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radiolarian species cover three successive stages, but with a relatively high proportion of single-interval taxa (ca. 57%). The base of the Llandovery is clearly depleted in radiolarians and the post-Hirnantian (end-Ordovician
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major extinction event) faunas only show few species of Haplotaeniatidae (e.g. Haplotaeniatum aperturatum, Orbiculopylorum adobensis, O. marginatum), Rotasphaeridae (e.g. Secuicollacta glaebosa, S. gliris), and
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Haplentactinidae (Syntagentactinia afflicta). During the Llandovery, the family Haplotaeniatidae rapidly diversified and became one of the major radiolarian families. The same holds true for the families Rotasphaeridae and Palaeoscenidiidae, which were also well represented during the upper Silurian. The families Inaniguttidae, Entactiniidae, Palaeoactinosphaeridae, and “Sponguridae” diversified during the Wenlock, Ludlow and Přídolí. Interestingly, Rotasphaeridae, Palaeoscenidiidae and Inaniguttidae, which are well represented during the entire Silurian, show an interval devoid of any representatives, or at least a very low taxonomic richness during the Homerian. A faunal turnover during the Wenlock to Ludlow stages is also visible, with different species occurring before and after this interval. The family Haplotaeniatidae went almost extinct just before the Homerian while the families Palaeoactinosphaeridae and “Sponguridae” diversified after this low
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ACCEPTED MANUSCRIPT period. Global diversity curves for radiolarian species through the eight Silurian stages are shown in Figure 2. Only ratios (per Myr) will be discussed herein, because raw results are largely influenced by the duration of the stages, which can exhibit significant discrepancies for the Silurian period (compare Figure 2 and Appendix E). Species richness (Dnorm, Drt-, and Dsib) is characterized by a plateau of moderate values following its lowest value in the Rhuddanian and interrupted by a peak of highest diversity in the Gorstian. The number of crossover
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species (Dover) constitutes on average a third of the taxonomic richness and is relatively low during the Telychian and Gorstian. In contrast, the number of single-interval taxa (Dsgl) is often a minor component, except in the
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Telychian and Gorstian, where they constitute more than a third of the total taxonomic richness. Interestingly,
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the Rhuddanian exhibits a very low diversity, following the Hirnantian biotic crisis.
With regard to extinction and origination rates (Fig. 2; compare Appendix E for raw values), the global
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trend for the entire Silurian is a fairly muted pattern that is interrupted only by a sharp turnover during the Gorstian (Tsbe and Trte). This turnover event corresponds to a peak of origination in the Gorstian compared to the
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older Homerian and a peak of extinction compared to the younger Ludfordian. Otherwise, extinction rates per Myr (Erte and Esbe) are rather constant after a slight increase during the early Silurian. Origination rates per Myr (Orte and Osbe) show a protracted decrease during the entire Silurian with the exception of this Gorstian pulse.
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Poly-cohorts of survivorship and prenascence produce almost parallel and relatively straight curves (Fig. 3),
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indicating that rates of origination and extinction are relatively constant throughout the Silurian. The polycohorts can nevertheless be clustered in two groups indicating change in rates around the Telychian and
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Homerian, thus reflecting the two turnover peaks shown by raw values of diversity (Appendix E). The number of studies in each of the stratigraphic intervals considered is irregular and particularly low
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for the Rhuddanian and the Ludfordian (Appendix C). Despite the small number of source studies for some intervals, the correlation (Fig. 4) of taxonomic (global species per stage) and monographic (references per stage) richness is low and not significant (Rrho = 0.38; prho = 0.352).
4. Discussion
The synthetic range charts (Appendices B, C, and D) show that chronostratigraphically well-constrained studies of Silurian radiolarians remain rare in general and are unevenly distributed in space and time. Hence,
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ACCEPTED MANUSCRIPT much effort remains to be made in acquiring more primary data on Silurian radiolarians before more robust and detailed analyses can be made, especially for the Rhuddanian and the Ludfordian, as well as for regions outside North America. Interestingly, most of the studies conducted for the Silurian have a "Laurentian" association (Fig. 1 and Appendix F; North America: Alaska, Nevada, Texas and Canada). It has to be noted that diversity and abundance of radiolarians in the fossil record largely depend on taphonomic conditions (De Wever et al., 1994). Radiolarians extracted from carbonate rocks in the Paleozoic, such as the Silurian assemblages from the
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Canadian Arctic, are unusually abundant and well preserved; thus, the lower Silurian assemblages described from Canadian localities may be partly responsible for inflating the diversity in the pre-Homerian faunas. Further
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in-depth studies are required to acquire a more complete perspective for radiolarian distribution in time and
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space based on occurrence data coming from other regions around the world. Nevertheless, Silurian radiolarian faunas are considered to be rather cosmopolitan (Noble and Maletz, 2000; Tetard et al., 2014b) underscoring the
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need for more sampling of poorly studied intervals (e.g. Noble et al., 1998; Tetard et al., 2015) in order to achieve better understanding of diversity and evolutionary patterns in Silurian radiolarians. Considering the low
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number of radiolarian studies throughout the entire Silurian, the results of this biodiversity study should be regarded with some caution. They appear to be independent of monographic disparity between stages because comparison of the diversity indices with the number of published studies (Fig. 4; also compare Fig. 2 and
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Appendix E) shows that they are not correlated. Besides, the peak in taxonomic richness during the Gorstian is
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associated with only two published studies, whereas the interval that spans the Homerian crisis is reported in four of them. Low reference numbers may be attributable to the lowest diversity, that occurs in the Rhuddanian
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where the number of source studies is the least; however; the low taxonomic richness is consistent with the faunal recovery following the Hirnantian mass extinction. Therefore, diversity patterns of Silurian radiolarians
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do not appear to be directly influenced by the number of studies within given stratigraphic interval. Also, of the 69 species ranging beyond a single stage, only 15 (ca. 22%) involve inferred ranges. This implies that their fossil record is relatively consistent and that very few assumptions were made in the calculation of diversity indices. The results clearly reflect variations in radiolarian diversity for the entire Silurian, and demonstrate some significant global trends. Firstly, diversity was lowest during the Rhuddanian (Fig. 2) before quickly reaching a plateau of moderate values in the Aeronian. Therefore, the Rhuddanian is characteristic of the faunal recovery following the end-Ordovician crisis (Loydell, 2007; Munnecke et al., 2010). After this relatively "short" recovery (a single 3 Myr long stage), a moderate plateau with low, but regular, extinction and origination rates, from the Aeronian to the Homerian (thus covering four stages) is observed. A sudden peak of diversity occurred
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ACCEPTED MANUSCRIPT during the Gorstian (Fig. 2), immediately following the Homerian low. This pattern can be explained by a major pulse in origination which, combined with a slight increase in extinction, was responsible for a high rate of faunal turnover, leading to the quickest and highest rate of diversification for the Silurian radiolarians. Radiolarian and graptolite communities are likely to respond to similar environmental perturbations leading to bio-events within the planktic realm. Indeed, graptolites (and more particularly Graptoloids; Cooper et al., 2014) can also be used to investigate the biotic response of marine planktic organisms to environmental
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perturbations during the Paleozoic. The habitat of this well-studied group was linked to several oceanographic parameters such as water masses circulation, upwellings and quality/quantity of available nutrients, as well as
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temperature gradients, which are all related to global climate (Cooper et al., 2014 and references therein).
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Interestingly, roughly similar taxonomic richness patterns were observed for graptolite faunas (Fig. 5). A global long-term decrease throughout the entire Silurian period, is characterized by a recovery phase in its early stages
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reaching a maximum number of species in the Aeronian. This was followed by a protracted decrease until a low diversity interval associated with the Mulde event occurred in the Homerian. Finally a sudden high diversity
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peak occurred during the Gorstian (Lenz et al., 2006; Cooper et al., 2014; Trotter et al., 2016). A major crisis in graptolite faunas occurred during the early Homerian (LEE: Lundgreni Extinction Event) and led to very low number of species during the late Homerian. A major extinction event is also reported in the middle Silurian for
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conodont species (Prothero, 2013). Following this LEE, radiolarians were reported to be very sporadically
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distributed in the Arctic Canada (Lenz et al., 2006), before the diversity remarkably increased again during the Gorstian stage. This Ludlow origination event, even though reported in other major marine groups (e.g.
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graptolites, non-stromatoporoid sponges; Muir et al., 2013; Cooper et al., 2014; Trotter et al., 2016) is relatively poorly studied as most studies focused on extinction rather than diversification events. Environmental changes during the Silurian that may have triggered changes in radiolarian biodiversity
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potentially can be distinguished by investigating carbon isotope global excursions (δ13C; Noble et al., 2005; Munnecke et al., 2010; Cramer et al., 2011). During the Silurian, three major positive excursions are recorded (Calner, 2008 and references therein; Munnecke et al., 2010; Trotter et al., 2016). They correspond to important biotic events (Ireviken, Mulde, and Lau events) affecting several marine groups, from planktic to shallow water benthic organisms. Due to its stratigraphic position, the Homerian radiolarian extinction observed in the results is likely to be associated with the Mulde event, which corresponds to a faunal turnover affecting many pelagic groups (i.e. graptolites, acritarchs, conodonts, chitinozoans, and radiolarians; Lenz et al., 2006; Calner, 2008; Cooper et al., 2014). Munnecke et al. (2010) pointed out that no simple explanations are available for the
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ACCEPTED MANUSCRIPT Silurian biotic crises, however, the Mulde event was recorded worldwide by a δ13C isotopic excursion (Calner, 2008), and coincided with a substantial marine regression. Organic-rich shale deposits retrieved worldwide are likely to have been related to widespread anoxia (Calner, 2008) that is already known to severely affect radiolarian diversity (e.g. Cretaceous OAEs; De Wever et al., 2003). Graptolite diversity patterns were also assumed to be linked with significant temperature changes (Cooper et al., 2014). A major positive excursion in the isotopic composition of conodont microfossils (δ18Ophos) indicates a cooling phase associated with the
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Homerian glaciation and correlated with a very low number of graptolite species, while a complete graptolite turnover during the Gorstian was probably linked with a significant climate warming with the highest
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temperatures known from the Silurian (Trotter et al., 2016).
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5. Conclusion
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An analysis of the radiolarian diversity for the entire Silurian period has been carried out by examining all well-dated occurrences of radiolarians reported in the literature in a common chronostratigraphic framework. Silurian radiolarian ranges were thus produced as well as several analyses investigating changes in biodiversity
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dynamics for the studied period. Both the charts and performed analyses depict a diversification that took place
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during the early Silurian, and rapidly reached a plateau. Diversity levels decreased during the Homerian stage due to a combination of increased extinction and low origination. This biotic crisis is possibly correlated with the
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Mulde event (positive excursion in carbon isotope). Diversity levels peaked suddenly during the Gorstian. Several tests were conducted in order to check the consistency of data and results and diversity values seem
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uncorrelated with the degree of stratigraphic coverage of the data. Nevertheless, further work is needed in order to fill stratigraphic gaps with additional well-dated collections, and examine the degree of correspondance in biodiversity dynamics between radiolarians and other pelagic groups, especially across the major biotic events recognized during the Silurian period.
Acknowledgements
Thanks to the editor Paul Wilson and the reviewers for their constructive remarks that improved the
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ACCEPTED MANUSCRIPT original manuscript of this paper. The authors thank the Région Hauts-de-France, and the Ministère de l’Enseignement Supérieur et de la Recherche (CPER Climibio), and the European Fund for Regional Economic Development for their financial support. The research of Paula Noble was also funded in part by an International Activities Grant of the University of Nevada Reno and a visiting professorship sponsored by the University of
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Lille – Sciences and Technologies.
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Formation of east-central Alaska and the new family Haplotaeniatumidae. J. Paleontol. 76, 941–964.
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Figure captions
Figure 1. Paleogeographic map showing radiolarian localities integrated in this analysis. Numbers in parentheses
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indicate the number of stages covered by these localities.
Figure 2. Global indices of taxonomic richness and taxonomic changes (rates per Myr) of Silurian radiolarians
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(see text for the definition of the various taxonomic richness indices).
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Figure 3. Poly-cohort analyses (cohort survivorship and cohort prenascence) for the Silurian stages.
Figure 4. Correlation (Rtau and Rrho) of taxonomic diversity (number of species per stage; sampled-in-bin diversity Dsib) and authorship (number of references per stage).
Figure 5. Comparison of the diversity of radiolarians (this study) and graptolites (Cooper et al., 2014) during the Silurian.
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Martin Tetard, Claude Monnet, Paula J. Noble, Taniel Danelian PII: DOI: Reference:
S0012-8252(17)30186-1 doi: 10.1016/j.earscirev.2017.07.011 EARTH 2459
To appear in:
Earth-Science Reviews
Received date: Revised date: Accepted date:
5 April 2017 21 June 2017 24 July 2017
Please cite this article as: Martin Tetard, Claude Monnet, Paula J. Noble, Taniel Danelian , Biodiversity patterns of Silurian Radiolaria, Earth-Science Reviews (2017), doi: 10.1016/ j.earscirev.2017.07.011
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Biodiversity patterns of Silurian Radiolaria
Martin Tetard *, a, b, Claude Monnet a, Paula J. Noble a, c, Taniel Danelian a
Univ. Lille, CNRS, UMR 8198 – Evo-Eco-Paleo, F-59000 Lille, France
b
Aix Marseille Univ, CNRS, IRD, Coll France, CEREGE, Aix-en-Provence, France
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University of Nevada, Department of Geological Sciences, Mackay School of Mines, Reno, NV 89557-0138,
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a
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USA
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AUTHOR INFORMATION
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*Corresponding author. Email: [email protected]
Email addresses of all authors: [email protected] (M. Tetard), [email protected] (C. Monnet),
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[email protected] (P.J. Noble), [email protected] (T. Danelian)
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ACCEPTED MANUSCRIPT Abstract Data analysis of all published and well-dated Silurian radiolarian localities was conducted with the goal of revealing long-term patterns in Silurian radiolarian biological diversity. The chronostratigraphic distribution of 161 species was compiled from 25 publications, each selected because of their independent age control. The pattern and dynamics of changes in biodiversity are described using indices that allow for the assessment of changes in taxonomic richness through time. Following the Hirnantian (end-Ordivician) mass extinction, the
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Rhuddanian stage records very low levels of diversity, which then increase gradually throughout the Llandovery series and reach a maximum by the Sheinwoodian stage, before decreasing during the Homerian, and finally,
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rebounding during the Gorstian stage. The early Silurian (Llandovery) appears to be an interval during which
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few species went extinct, although the number of last occurrences increases progressively to reach a peak in the Ludfordian. At the same time first occurrences progressively decrease and are relatively low during the Silurian.
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Only the Gorstian is marked by a sudden increase in origination. The early Silurian is an interval of faunal recovery from the end-Ordovician mass extinction event. Similarly, the Gorstian stage is characterized by a
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recovery following the Homerian low in radiolarian diversity that may be correlated with the C. lundgreni extinction event, which affected a number of other pelagic groups (e.g. graptolites, acritarchs, conodonts, and
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chitinozoans), and with the Mulde event, which coincides with a 4.6‰ positive excursion of the δ13C curve.
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Keywords
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Radiolaria, Paleozoic, paleobiodiversity, macroevolution, biodiversification, taxonomic richness
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ACCEPTED MANUSCRIPT 1. Introduction
Since the appearance of life, Earth’s history has been marked by mass extinctions punctuating periods of relative stability (Raup, 1972, 1976; Sepkoski et al., 1981; Raup and Sepkoski, 1982; Sepkoski, 1984; Alroy, 2008; Alroy et al., 2008; Escarguel et al., 2011). The investigation of such events and of the global mechanisms triggering them may provide some insights into future ecological consequences of our changing world (Alroy et
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al., 2008 and references therein; Sepkoski 1997). Understanding of the Silurian period has evolved over the last few decades (Munnecke et al., 2010). The traditional view for the early Silurian is that of a warm and relatively
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calm period in Earth history, with marine communities progressively recovering from the Hirnantian (end-
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Ordivician) mass extinction (Calner, 2008). However, later studies suggest that the Silurian experienced substantial and rapid climatic and environmental fluctuations, as indicated by the large degree of perturbations
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observed in high resolution C and O isotopic records (Calner, 2008; Munnecke et al., 2010; Gradstein et al., 2012 and references therein), accompanied by major biotic turnovers and extinction events. Many of the biotic
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events cross-cut ecological boundaries and affected well-established groups (Munnecke et al., 2003, 2010; Lenz et al., 2006; Trotter et al., 2016): planktic (acritarchs, graptolites), benthic (brachiopods, trilobites) and nektonic (conodonts), investigation of whose evolution is of primary importance for understanding Silurian
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paleobiodiversity dynamics.
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Most of these groups are also widely used (globally or locally) for Silurian biostratigraphy (Ogg et al., 2016). Marine micro-organisms such as radiolarians represent a significant part of planktic communities at the
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base of marine food webs and are very sensitive to changes in ecological conditions (Lazarus, 2005). Their diversity patterns can thus be used to reconstruct biotic events. However, there are few works that have studied
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radiolarian diversity trends through geological time. The few studies that have been conducted have mainly focused on particular time intervals such as the Permian/Triassic and Cretaceous/Paleogene boundary mass extinctions, or the middle Jurassic to early Cretaceous of the Tethys ocean (Danelian and Johnson, 2001; De Wever et al., 2003; Kiessling and Danelian, 2011). Concerning the Silurian period, most published studies have focused on faunal recovery from the end-Ordovician (Hirnantian) crisis for several groups (e.g. Krug and Patzkowsky, 2004) but excluding the radiolarians. To help fill this knowledge gap, this study focuses on paleodiversity dynamics of the radiolarian faunas during the entire Silurian period. We present a database of Silurian radiolarian occurrences, including a comprehensive dataset at the species level, in order to approximate their standing diversity and to identify
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ACCEPTED MANUSCRIPT biodiversity and evolutionary trends. These patterns are also tested for inherent biases in the database.
2. Material and methods 2.1. Dataset
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A global and exhaustive dataset of Silurian radiolarian occurences was established through surveying the available literature. This survey yielded an inventory of 25 publications that demonstrated sufficient
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chronostratigraphic information to calibrate radiolarian occurrences at the stage level. The constructed dataset
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(Appendix A) contains a list of identified taxa at the species rank for each sample described within a given reference. Samples reported in these references were either dated by fossils other than radiolarians (e.g.
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graptolites) or by absolute dating (e.g. U/Pb SHRIMP). The time calibration of the stages used for the biodiversity analysis is based on the framework established by Ogg et al. (2016). The age of some samples has
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been revised or clarified from the original works when subsequent dating has become available. For example, the age of the Spongocoelia parvus–S. kamitakarensis assemblage regarded by Furutani (1990) as either late Ludlow (in the abstract) or early Ludlow (in the discussion), or mid-Ludlow according to Noble (1994), is here
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considered as late Ludlow based on Nuramkhaan et al. (2013), who made a compelling case for revision. Thus,
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the age of some assemblages may be different from that given in the original publication, but the updated age is always justified by reference to more recent papers. Samples or references were excluded from the analysis if the
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age uncertainty was too large (e.g. Nazarov and Ormiston, 1993) or if most of the specimens were not identified to the species level (e.g. Wakamatsu, 1990; Gorka, 1994; Aitchison et al., 1996; Kurihara and Sashida, 2000b).
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Also, taxonomic assignments of species were reviewed in the original publications and species names were harmonized to remove nomenclatural artifacts that might impede accurate measures of radiolarian diversity. This creates a taxonomic framework that reflects the current state of research with as much consistency and as little redundancy as possible. The final dataset (after cleaning up of uncertain taxa) contains 9 families, 51 genera and 161 species. Most of the data come primarily from Arctic Canada (9 references) and from Japan (7), and sporadically from France, Sweden, Kazakhstan, Texas, Nevada, Alaska, Germany and England (Fig. 1). Therefore, it covers 10 areas, eight of which were situated in tropical paleolatitudes (between 30° N and 30° S) and only two in the midhigh latitudes (near 60° S).
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2.2. Biodiversity metrics
The dataset analyzed in this study (Appendix A) contains only incidence data (i.e. presence/absence) because abundance data are rarely available and were only present in a handful of the surveyed publications. Consequently, biodiversity metrics based on abundance data and correction for sampling bias such as rarefaction
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analyses (Foote, 1992) and subsampling methods (Alroy, 2010) cannot be used in this analysis. This study focuses on taxonomic richness measured at the species rank. The taxa counted herein include also reports of
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species assigned under open nomenclature (e.g. as ‘sp. A’) or with an uncertain specific identification (e.g. ‘cf.’).
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The biodiversity analysis is computed at the chronostratigraphic rank of the eight Silurian stages (Ogg et al., 2016). The choice of these stratigraphic bins was a compromise guided by the resolution required to address our
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research question, the available data, and the maximal precision with which data can be attributed to a given stratigraphic interval of the Silurian (a significant number of references did not date their samples down to the
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biozone).
Biodiversity dynamics through time with incidence data can be estimated by multiple approaches, such as taxonomic richness indices, changes in richness (origination, extinction), and poly-cohort analysis, which are
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processed in this study. The computed analysis was performed by using the scientific environment R (R Core
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Team 2016) version 3.3.0 and with the package ‘epaleo’ (C. Monnet, 2015, unpublished; for applications using this package, see Nowak et al., 2015 and Amberg et al., 2016).
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The actual number of coexisting taxa is the standing diversity, which can only be estimated for paleontological data. Based on incidence taxa, several taxonomic richness indices can be calculated depending
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on the relative weights according to each class of taxa with regard to their occurrence in and around a stratigraphic interval. Taxa are counted as present in a stratigraphic interval in one of four ways (Foote, 2000; Alroy, 2010): as crossovers ranging through the entire interval (sampled or not in it); ranging into and going extinct in that interval; originating within the interval and ranging beyond its upper boundary; and as singleinterval, with a range confined to an interval, meaning that they originate and go extinct within the interval. The sampled-in-bin diversity (Dsib) provides the total count of taxa actually documented from a given stratigraphic interval. This index commonly underestimates diversity due to the incompleteness of the fossil record and sampling bias. Total diversity (Drt-: range-through diversity) also counts all the taxa present in the interval, but it is also calculated by interpolation of discontinuous taxon ranges from established occurrences (Foote, 2000), i.e.
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ACCEPTED MANUSCRIPT taxa not recorded in an interval are counted as being present if they occur in intervals below and above. With this approach, single-interval taxa can be included (Drti) or excluded (Drte). With complete data, total diversity is likely to exceed the standing diversity at any specific point in time, because it does not account for extinctions within an interval (Cooper, 2004). Normalized diversity (Dnorm) is calculated as the number of species ranging throughout the interval (Dover), plus half the number of taxa that originate and/or become extinct in that stage, plus half of those that are confined to the interval itself (D sgl) (Sepkoski, 1975; Cooper, 2004). According to
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Cooper (2004), normalized diversity is a good approximation of the mean standing diversity in a stratigraphic bin.
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Indices of origination and extinction represent, respectively, the number of species originating (Orte and
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Osbe: origination of range-thru excluding single-interval taxa and origination of sampled-in-bin excluding singleinterval taxa, respectively) and becoming extinct (Erte and Esbe) in a stratigraphic interval. Turnover (Trte and Tsbe)
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in an interval is the sum of origination and extinction events, whereas net changes (Crte and Csbe) correspond to origination minus extinction.
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The use of stages as the stratigraphic intervals in this analysis implies that these are inevitably of different durations, which may partly bias diversity counts: longer bins may have a higher taxonomic richness than shorter bins simply because they are sampling longer intervals, while at the same time blurring short-term
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excursions. As the duration of Silurian stages may vary from 1.8 Myr (Gorstian) to 5.1 Myr (Telychian; see Ogg
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et al., 2016) a notable effect may be expected. To correct for a possible bias resulting from these unequal interval lengths, rates per Myr for all diversity indices have been computed. The efficiency of this correction relies on the
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amount and precision of available radio-isotopic ages for this period (see Melchin et al., 2012, fig. 21.12). Poly-cohort analysis is a common tool in paleontology to evaluate evenness of extinction and
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origination rates (Raup, 1978; Foote, 2001; Monnet et al., 2003). Poly-cohort survivorship measures the percentage of species in a cohort, i.e. species present in a given stratigraphic interval that are still present in later intervals. In contrast, poly-cohort prenascence (backward survivorship) measures the proportion of a cohort present in earlier intervals. Poly-cohorts of survivorship and of prenascence are calculated for all stratigraphic bins considered herein. The slope of the cohort curves then represents the rate of extinction or origination for each cohort, with a linear curve (on a logarithmic scale) implying constant rates, while changes over time or between cohorts can reveal changes in rates or biases. The possible influence of sampling bias is evaluated by calculating the Spearman's ρ (rho) and the Kendall’s τ (tau) correlations between the computed diversity indices and the number of studies per interval.
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ACCEPTED MANUSCRIPT These are standard non-parametric rank order correlation coefficients (e.g. Press et al., 1992) commonly used in paleontology (e.g. Dunhill et al., 2012; Na and Kiessling, 2015). The importance of correlation is assessed by Rrho and Rtau values, which vary between -1 and 1 for perfect negative and positive correlation, respectively, with 0 indicating absence of correlation. The statistical significance is given by the probability value p, which is derived from permutation tests. A correlation is accepted as strong if the coefficient is high (> 0.75) and
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significant if the probability value is low (< 0.05).
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3. Results
The constructed dataset used for the biodiversity analysis (Appendix A) contains incidence data (i.e.
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presence/absence) of 161 species distributed in 8 stratigraphic intervals (stages) compiled from 25 source studies (references). The analysis of this dataset enables reconstructing a synthetic occurrence range chart (Appendix B)
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in which species are ordered by family membership and then by appearance, as well as a chart of stratigraphic coverage of source studies (Appendix C). These charts clearly show that some intervals are well documented, such as the Telychian, while other intervals are very poorly studied, such as the Rhuddanian and Ludfordian.
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Also, the synthetic chronostratigraphic range of radiolarian species (Appendix D) shows that on average
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radiolarian species cover three successive stages, but with a relatively high proportion of single-interval taxa (ca. 57%). The base of the Llandovery is clearly depleted in radiolarians and the post-Hirnantian (end-Ordovician
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major extinction event) faunas only show few species of Haplotaeniatidae (e.g. Haplotaeniatum aperturatum, Orbiculopylorum adobensis, O. marginatum), Rotasphaeridae (e.g. Secuicollacta glaebosa, S. gliris), and
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Haplentactinidae (Syntagentactinia afflicta). During the Llandovery, the family Haplotaeniatidae rapidly diversified and became one of the major radiolarian families. The same holds true for the families Rotasphaeridae and Palaeoscenidiidae, which were also well represented during the upper Silurian. The families Inaniguttidae, Entactiniidae, Palaeoactinosphaeridae, and “Sponguridae” diversified during the Wenlock, Ludlow and Přídolí. Interestingly, Rotasphaeridae, Palaeoscenidiidae and Inaniguttidae, which are well represented during the entire Silurian, show an interval devoid of any representatives, or at least a very low taxonomic richness during the Homerian. A faunal turnover during the Wenlock to Ludlow stages is also visible, with different species occurring before and after this interval. The family Haplotaeniatidae went almost extinct just before the Homerian while the families Palaeoactinosphaeridae and “Sponguridae” diversified after this low
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ACCEPTED MANUSCRIPT period. Global diversity curves for radiolarian species through the eight Silurian stages are shown in Figure 2. Only ratios (per Myr) will be discussed herein, because raw results are largely influenced by the duration of the stages, which can exhibit significant discrepancies for the Silurian period (compare Figure 2 and Appendix E). Species richness (Dnorm, Drt-, and Dsib) is characterized by a plateau of moderate values following its lowest value in the Rhuddanian and interrupted by a peak of highest diversity in the Gorstian. The number of crossover
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species (Dover) constitutes on average a third of the taxonomic richness and is relatively low during the Telychian and Gorstian. In contrast, the number of single-interval taxa (Dsgl) is often a minor component, except in the
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Telychian and Gorstian, where they constitute more than a third of the total taxonomic richness. Interestingly,
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the Rhuddanian exhibits a very low diversity, following the Hirnantian biotic crisis.
With regard to extinction and origination rates (Fig. 2; compare Appendix E for raw values), the global
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trend for the entire Silurian is a fairly muted pattern that is interrupted only by a sharp turnover during the Gorstian (Tsbe and Trte). This turnover event corresponds to a peak of origination in the Gorstian compared to the
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older Homerian and a peak of extinction compared to the younger Ludfordian. Otherwise, extinction rates per Myr (Erte and Esbe) are rather constant after a slight increase during the early Silurian. Origination rates per Myr (Orte and Osbe) show a protracted decrease during the entire Silurian with the exception of this Gorstian pulse.
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Poly-cohorts of survivorship and prenascence produce almost parallel and relatively straight curves (Fig. 3),
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indicating that rates of origination and extinction are relatively constant throughout the Silurian. The polycohorts can nevertheless be clustered in two groups indicating change in rates around the Telychian and
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Homerian, thus reflecting the two turnover peaks shown by raw values of diversity (Appendix E). The number of studies in each of the stratigraphic intervals considered is irregular and particularly low
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for the Rhuddanian and the Ludfordian (Appendix C). Despite the small number of source studies for some intervals, the correlation (Fig. 4) of taxonomic (global species per stage) and monographic (references per stage) richness is low and not significant (Rrho = 0.38; prho = 0.352).
4. Discussion
The synthetic range charts (Appendices B, C, and D) show that chronostratigraphically well-constrained studies of Silurian radiolarians remain rare in general and are unevenly distributed in space and time. Hence,
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ACCEPTED MANUSCRIPT much effort remains to be made in acquiring more primary data on Silurian radiolarians before more robust and detailed analyses can be made, especially for the Rhuddanian and the Ludfordian, as well as for regions outside North America. Interestingly, most of the studies conducted for the Silurian have a "Laurentian" association (Fig. 1 and Appendix F; North America: Alaska, Nevada, Texas and Canada). It has to be noted that diversity and abundance of radiolarians in the fossil record largely depend on taphonomic conditions (De Wever et al., 1994). Radiolarians extracted from carbonate rocks in the Paleozoic, such as the Silurian assemblages from the
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Canadian Arctic, are unusually abundant and well preserved; thus, the lower Silurian assemblages described from Canadian localities may be partly responsible for inflating the diversity in the pre-Homerian faunas. Further
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in-depth studies are required to acquire a more complete perspective for radiolarian distribution in time and
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space based on occurrence data coming from other regions around the world. Nevertheless, Silurian radiolarian faunas are considered to be rather cosmopolitan (Noble and Maletz, 2000; Tetard et al., 2014b) underscoring the
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need for more sampling of poorly studied intervals (e.g. Noble et al., 1998; Tetard et al., 2015) in order to achieve better understanding of diversity and evolutionary patterns in Silurian radiolarians. Considering the low
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number of radiolarian studies throughout the entire Silurian, the results of this biodiversity study should be regarded with some caution. They appear to be independent of monographic disparity between stages because comparison of the diversity indices with the number of published studies (Fig. 4; also compare Fig. 2 and
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Appendix E) shows that they are not correlated. Besides, the peak in taxonomic richness during the Gorstian is
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associated with only two published studies, whereas the interval that spans the Homerian crisis is reported in four of them. Low reference numbers may be attributable to the lowest diversity, that occurs in the Rhuddanian
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where the number of source studies is the least; however; the low taxonomic richness is consistent with the faunal recovery following the Hirnantian mass extinction. Therefore, diversity patterns of Silurian radiolarians
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do not appear to be directly influenced by the number of studies within given stratigraphic interval. Also, of the 69 species ranging beyond a single stage, only 15 (ca. 22%) involve inferred ranges. This implies that their fossil record is relatively consistent and that very few assumptions were made in the calculation of diversity indices. The results clearly reflect variations in radiolarian diversity for the entire Silurian, and demonstrate some significant global trends. Firstly, diversity was lowest during the Rhuddanian (Fig. 2) before quickly reaching a plateau of moderate values in the Aeronian. Therefore, the Rhuddanian is characteristic of the faunal recovery following the end-Ordovician crisis (Loydell, 2007; Munnecke et al., 2010). After this relatively "short" recovery (a single 3 Myr long stage), a moderate plateau with low, but regular, extinction and origination rates, from the Aeronian to the Homerian (thus covering four stages) is observed. A sudden peak of diversity occurred
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ACCEPTED MANUSCRIPT during the Gorstian (Fig. 2), immediately following the Homerian low. This pattern can be explained by a major pulse in origination which, combined with a slight increase in extinction, was responsible for a high rate of faunal turnover, leading to the quickest and highest rate of diversification for the Silurian radiolarians. Radiolarian and graptolite communities are likely to respond to similar environmental perturbations leading to bio-events within the planktic realm. Indeed, graptolites (and more particularly Graptoloids; Cooper et al., 2014) can also be used to investigate the biotic response of marine planktic organisms to environmental
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perturbations during the Paleozoic. The habitat of this well-studied group was linked to several oceanographic parameters such as water masses circulation, upwellings and quality/quantity of available nutrients, as well as
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temperature gradients, which are all related to global climate (Cooper et al., 2014 and references therein).
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Interestingly, roughly similar taxonomic richness patterns were observed for graptolite faunas (Fig. 5). A global long-term decrease throughout the entire Silurian period, is characterized by a recovery phase in its early stages
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reaching a maximum number of species in the Aeronian. This was followed by a protracted decrease until a low diversity interval associated with the Mulde event occurred in the Homerian. Finally a sudden high diversity
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peak occurred during the Gorstian (Lenz et al., 2006; Cooper et al., 2014; Trotter et al., 2016). A major crisis in graptolite faunas occurred during the early Homerian (LEE: Lundgreni Extinction Event) and led to very low number of species during the late Homerian. A major extinction event is also reported in the middle Silurian for
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conodont species (Prothero, 2013). Following this LEE, radiolarians were reported to be very sporadically
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distributed in the Arctic Canada (Lenz et al., 2006), before the diversity remarkably increased again during the Gorstian stage. This Ludlow origination event, even though reported in other major marine groups (e.g.
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graptolites, non-stromatoporoid sponges; Muir et al., 2013; Cooper et al., 2014; Trotter et al., 2016) is relatively poorly studied as most studies focused on extinction rather than diversification events. Environmental changes during the Silurian that may have triggered changes in radiolarian biodiversity
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potentially can be distinguished by investigating carbon isotope global excursions (δ13C; Noble et al., 2005; Munnecke et al., 2010; Cramer et al., 2011). During the Silurian, three major positive excursions are recorded (Calner, 2008 and references therein; Munnecke et al., 2010; Trotter et al., 2016). They correspond to important biotic events (Ireviken, Mulde, and Lau events) affecting several marine groups, from planktic to shallow water benthic organisms. Due to its stratigraphic position, the Homerian radiolarian extinction observed in the results is likely to be associated with the Mulde event, which corresponds to a faunal turnover affecting many pelagic groups (i.e. graptolites, acritarchs, conodonts, chitinozoans, and radiolarians; Lenz et al., 2006; Calner, 2008; Cooper et al., 2014). Munnecke et al. (2010) pointed out that no simple explanations are available for the
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ACCEPTED MANUSCRIPT Silurian biotic crises, however, the Mulde event was recorded worldwide by a δ13C isotopic excursion (Calner, 2008), and coincided with a substantial marine regression. Organic-rich shale deposits retrieved worldwide are likely to have been related to widespread anoxia (Calner, 2008) that is already known to severely affect radiolarian diversity (e.g. Cretaceous OAEs; De Wever et al., 2003). Graptolite diversity patterns were also assumed to be linked with significant temperature changes (Cooper et al., 2014). A major positive excursion in the isotopic composition of conodont microfossils (δ18Ophos) indicates a cooling phase associated with the
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Homerian glaciation and correlated with a very low number of graptolite species, while a complete graptolite turnover during the Gorstian was probably linked with a significant climate warming with the highest
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temperatures known from the Silurian (Trotter et al., 2016).
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5. Conclusion
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An analysis of the radiolarian diversity for the entire Silurian period has been carried out by examining all well-dated occurrences of radiolarians reported in the literature in a common chronostratigraphic framework. Silurian radiolarian ranges were thus produced as well as several analyses investigating changes in biodiversity
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dynamics for the studied period. Both the charts and performed analyses depict a diversification that took place
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during the early Silurian, and rapidly reached a plateau. Diversity levels decreased during the Homerian stage due to a combination of increased extinction and low origination. This biotic crisis is possibly correlated with the
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Mulde event (positive excursion in carbon isotope). Diversity levels peaked suddenly during the Gorstian. Several tests were conducted in order to check the consistency of data and results and diversity values seem
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uncorrelated with the degree of stratigraphic coverage of the data. Nevertheless, further work is needed in order to fill stratigraphic gaps with additional well-dated collections, and examine the degree of correspondance in biodiversity dynamics between radiolarians and other pelagic groups, especially across the major biotic events recognized during the Silurian period.
Acknowledgements
Thanks to the editor Paul Wilson and the reviewers for their constructive remarks that improved the
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ACCEPTED MANUSCRIPT original manuscript of this paper. The authors thank the Région Hauts-de-France, and the Ministère de l’Enseignement Supérieur et de la Recherche (CPER Climibio), and the European Fund for Regional Economic Development for their financial support. The research of Paula Noble was also funded in part by an International Activities Grant of the University of Nevada Reno and a visiting professorship sponsored by the University of
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Lille – Sciences and Technologies.
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Figure captions
Figure 1. Paleogeographic map showing radiolarian localities integrated in this analysis. Numbers in parentheses
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indicate the number of stages covered by these localities.
Figure 2. Global indices of taxonomic richness and taxonomic changes (rates per Myr) of Silurian radiolarians
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(see text for the definition of the various taxonomic richness indices).
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Figure 3. Poly-cohort analyses (cohort survivorship and cohort prenascence) for the Silurian stages.
Figure 4. Correlation (Rtau and Rrho) of taxonomic diversity (number of species per stage; sampled-in-bin diversity Dsib) and authorship (number of references per stage).
Figure 5. Comparison of the diversity of radiolarians (this study) and graptolites (Cooper et al., 2014) during the Silurian.
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